Effects of selective and non-selective inhibitors of nitric oxide synthase on morphine- and endomorphin-1-induced analgesia in acute and neuropathic pain in rats

Neuropharmacology

Volumn 75, Issue , 2013, Pages 445-457

  Makuch, Wioletta ^a   Mika, Joanna ^a   Rojewska, Ewelina ^a   Zychowska, Magdalena ^a   Przewlocka, Barbara ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

Mechanical allodynia; Neuropathic pain; Nitric oxide; Nitric oxide synthase; Nociception; Thermal hyperalgesia

Indexed keywords

1 (2 TRIFLUOROMETHYLPHENYL)IMIDAZOLE; 7 NITROINDAZOLE; COMPLEMENT COMPONENT C1Q; ENDOMORPHIN 1; INDUCIBLE NITRIC OXIDE SYNTHASE; MESSENGER RNA; MINOCYCLINE; MORPHINE; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; N(G) NITROARGININE METHYL ESTER; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CELL ACTIVATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; HYPERALGESIA; MALE; MICROGLIA; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PAIN; PAIN THRESHOLD; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SPINAL CORD; TAIL FLICK TEST;

% MPE; 1-(2-TRIFLUOROMETHYL-PHENYL)-IMIDAZOLE; 1400W; 7-NI; 7-NITROINDAZOLE; CCI; CGMP; CHRONIC CONSTRICTION INJURY; CYCLIC GUANOSINE MONOPHOSPHATE; DORSAL ROOT GANGLIA; DRG; EM-1; ENDOMORPHIN-1; I.T.; INTRATHECAL; L-NAME; M; MECHANICAL ALLODYNIA; MORPHINE; N-([3-(AMINOMETHYL)PHENYL]METHYL)ETHANIMIDAMIDE DIHYDROCHLORIDE (1400W DIHYDROCHLORIDE); NEUROPATHIC PAIN; NG-NITRO-L-ARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NO; NOCICEPTION; NOS; PERCENTAGE OF MAXIMAL POSSIBLE ANTINOCICEPTIVE EFFECT; THERMAL HYPERALGESIA; TRIM;

ANALGESICS, OPIOID; ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GANGLIA, SPINAL; INDAZOLES; MALE; MEMBRANE GLYCOPROTEINS; MORPHINE; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE SYNTHASE; OLIGOPEPTIDES; PAIN MEASUREMENT; RATS; RATS, WISTAR; RECEPTORS, COMPLEMENT; RNA, MESSENGER; SCIATICA; SPINAL CORD; TIME FACTORS;

EID: 84884879260     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.08.031     Document Type: Article

References (147)

1. K.O. Aley, G. McCarter, and J.D. Levine Nitric oxide signaling in pain and nociceptor sensitization in the rat J. Neurosci. 18 1998 7008 7014 (Pubitemid 28388029)
2. V.A. Alvarez, S. Arttamangkul, V. Dang, A. Salem, J.L. Whistler, M. Von Zastrow, D.K. Grandy, and J.T. Williams mu-Opioid receptors: ligand-dependent activation of potassium conductance, desensitization, and internalization J. Neurosci. 22 2002 5769 5776 (Pubitemid 35386500)
3. A.M. Babey, Y. Kolesnikov, J. Cheng, C.E. Inturrisi, R.R. Trifilletti, and G.W. Pasternak Nitric oxide and opioid tolerance Neuropharmacology 33 1994 1463 1470 (Pubitemid 24353742)
4. C.P. Bailey, D. Couch, E. Johnson, K. Griffiths, E. Kelly, and G. Henderson Mu-opioid receptor desensitization in mature rat neurons: lack of interaction between DAMGO and morphine J. Neurosci. 23 2003 10515 10520 (Pubitemid 37485264)
5. G.J. Bennett, and Y.K. Xie A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man Pain 33 1988 87 107
6. H.N. Bhargava, and G.M. Zhao Effect of nitric oxide synthase inhibition on tolerance to the analgesic action of D-Pen2, D-Pen5 enkephalin and morphine in the mouse Neuropeptides 30 1996 219 223 (Pubitemid 26267209)
7. H.N. Bhargava, J.T. Bian, and S. Kumar Mechanism of attenuation of morphine antinociception by chronic treatment with L-arginine J. Pharmacol. Exp. Ther. 281 1997 707 712 (Pubitemid 27203802)
8. H.N. Bhargava, and Y.J. Cao Effect of chronic administration of morphine, U-50, 488H and [D-Pen2, D-Pen5]enkephalin on the concentration of cGMP in brain regions and spinal cord of the mouse Peptides 18 1997 1629 1634 (Pubitemid 28133008)
9. H.N. Bhargava, S. Kumar, and M.J. Barjavel Kinetics properties of nitric oxide synthase in cerebral cortex and cerebellum of morphine tolerant mice Pharmacology 56 1998 252 256 (Pubitemid 28171778)
10. T.V. Bilfinger, A. Hartman, Y. Liu, H.I. Magazine, and G.B. Stefano Cryopreserved veins used for myocardial revascularization: a 5 year experience and a possible mechanism for their increased failure Ann. Thorac. Surg. 63 1997 1063 1069 (Pubitemid 27191661)
11. C. Blanchet, and C. Lüscher Desensitization of mu-opioid receptor-evoked potassium currents: initiation at the receptor, expression at the effector Proc. Natl. Acad. Sci. U. S. A. 99 2002 4674 4679 (Pubitemid 34286043)
12. C. Blanchet, M. Sollini, and C. Lüscher Two distinct forms of desensitization of G-protein coupled inwardly rectifying potassium currents evoked by alkaloid and peptide mu-opioid receptor agonists Mol. Cell Neurosci. 24 2003 517 523 (Pubitemid 37311313)
13. D.S. Bredt, and S.H. Snyder Nitric oxide, a novel neuronal messenger Neuron 8 1992 3 11
14. D.S. Bredt Nitric oxide signaling specificity-the heart of the problem J. Cell Sci. 116 Pt 1 2003 9 15 (Pubitemid 36113960)
15. N.T. Burford, L.M. Tolbert, and W. Sadee Specific G protein activation and μ-opioid receptor internalization caused by morphine, DAMGO and endomorphin I Eur. J. Pharmacol. 342 1998 123 126 (Pubitemid 28131354)
16. A. Christopoulos, and E.E. El-Fakahany The generation of nitric oxide by G protein-coupled receptors Life Sci. 64 1999 1 15 (Pubitemid 29012744)
17. R.W. Colburn, J.A. DeLeo, A.J. Rickman, M.P. Yeager, P. Kwon, and W.F. Hickey Dissociation of microglial activation and neuropathic pain behaviors following peripheral nerve injury in the rat J. Neuroimmunol. 79 1997 163 175 (Pubitemid 27502035)
18. T.M. Cunha, D. Roman-Campos, C.M. Lotufo, H.L. Duarte, G.R. Souza, W.A. Verri Jr., M.I. Funez, Q.M. Dias, I.R. Schivo, A.C. Domingues, D. Sachs, S. Chiavegatto, M.M. Teixeira, J.S. Hothersall, J.S. Cruz, F.Q. Cunha, and S.H. Ferreira Morphine peripheral analgesia depends on activation of the PI3Kgamma/AKT/nNOS/NO/KATP signaling pathway Proc. Natl. Acad. Sci. U. S. A. 107 2010 4442 4447
19. T.M. Dawson, and S.H. Snyder Gases as biological messengers: nitric oxide and carbon monoxide in the brain J. Neurosci. 14 1994 5147 5159 (Pubitemid 24279040)
20. J. De Alba, N.M. Clayton, S.D. Collins, P. Colthup, I. Chessell, and R.G. Knowles GW274150, a novel and highly selective inhibitor of the inducible isoform of nitric oxide synthase (iNOS), shows analgesic effects in rat models of inflammatory and neuropathic pain Pain 120 2006 170 181 (Pubitemid 43077180)
21. J.A. DeLeo, V.L. Tawfik, and M.L. LaCroix-Fralish The tetrapartite synapse: path to CNS sensitization and chronic pain Pain 122 2006 17 21
22. J.E. Devulder Could nitric oxide be an important mediator in opioid tolerance and morphine side effects? J.Clin. Anesth. 14 2002 83 86
23. J. Dortch-Carnes, and K.R. Randall Morphine-induced nitric oxide production in isolated, iris-ciliary bodies Exp. Eye Res. 89 2009 660 664
24. S.H. Ferreira, I.D. Duarte, and B.B. Lorenzetti The molecular mechanism of action of peripheral morphine analgesia: stimulation of the cGMP system via nitric oxide release Eur. J. Pharmacol. 201 1991 121 122
25. C.E. Fiallos-Estrada, W. Kummer, B. Mayer, R. Bravo, M. Zimmermann, and T. Herdegen Long-lasting increase of nitric oxide synthase immunoreactivity, NADPH-diaphorase reaction and c-JUN co-expression in rat dorsal root ganglion neurons following sciatic nerve transection Neurosci. Lett. 150 1993 169 173 (Pubitemid 23153679)
26. U. Forstermann, I. Gath, P. Schwarz, E.I. Closs, and H. Kleinert Isoforms of nitric oxide synthase: properties, cellular distribution and expressional control Biochem. Pharmacol. 50 1995 1321 1332
27. M.G. Garry, L.P. Walton, and M.A. Davis Capsaicin-evoked release of IR calcitonin gene-related peptide from the spinal cord is mediated by nitric oxide but not by cyclic GMP Brain Res. 861 2000 208 219 (Pubitemid 30173307)
28. J. Garthwaite Glutamate, nitric oxide and cell-cell signaling in the nervous system Trends Neurosci. 14 1991 60 67
29. C. Giordano, D. Siniscalco, D. Melisi, L. Luongo, A. Curcio, M. Soukupova, E. Palazzo, I. Marabese, M. De Chiaro, M.G. Rimoli, F. Rossi, S. Maione, and V. de Novellis The galactosylation of N(ω)-nitro-L-arginine enhances its anti-nocifensive or anti-allodynic effects by targeting glia in healthy and neuropathic mice Eur. J. Pharmacol. 656 2011 52 62
30. S.J. Gold, M.H. Han, A.E. Herman, Y.G. Ni, C.M. Pudiak, G.K. Aghajanian, R.J. Liu, B.W. Potts, S.M. Mumby, and E.J. Nestler Regulation of RGS proteins by chronic morphine in rat locus coeruleus Eur. J. Neurosci. 17 2003 971 980 (Pubitemid 36411594)
31. V. Granados-Soto, M.O. Rufino, L.D. Gomes Lopes, and S.H. Ferreira Evidence for the involvement of the nitric oxide-cGMP pathway in the antinociception of morphine in the formalin test Eur. J. Pharmacol. 340 1997 177 180 (Pubitemid 28022639)
32. N. Gresa-Arribas, C. Viéitez, G. Dentesano, J. Serratosa, J. Saura, and C. Solà Modelling neuroinflammation in vitro: a tool to test the potential neuroprotective effect of anti-inflammatory agents PLoS One 7 2012 e45227
33. Y. Guan, M. Yaster, S.N. Raja, and Y.X. Tao Genetic knockout and pharmacologic inhibition of neuronal nitric oxide synthase attenuate nerve injury-induced mechanical hypersensitivity in mice Mol. Pain 3 2007 29
34. H. Guhring, M. Görig, M. Ates, O. Coste, H.U. Zeilhofer, A. Pahl, K. Rehse, and K. Brune Suppressed injury-induced rise in spinal prostaglandin E2 production and reduced early thermal hyperalgesia in iNOS-deficient mice J. Neurosci. 20 2000 6714 6720
35. H. Guhring, I. Tegeder, J. Lötsch, A. Pahl, U. Werner, P.W. Reeh, K. Rehse, K. Brune, and G. Geisslinger Role of nitric oxide in zymosan induced paw inflammation and thermal hyperalgesia Inflamm. Res. 50 2001 83 88 (Pubitemid 32210148)
36. B.C. Hains, C.Y. Saab, J.P. Klein, M.J. Craner, and S.G. Waxman Altered sodium channel expression in second-order spinal sensory neurons contributes to pain after peripheral nerve injury J. Neurosci. 24 2004 4832 4839 (Pubitemid 38668207)
37. J.E. Haley, A.H. Dickenson, and M. Schachter Electrophysiological evidence for a role of nitric oxide in prolonged chemical nociception in the rat Neuropharmacology 31 1992 251 258
38. R.L. Handy, P. Wallace, Z.A. Gaffen, K.J. Whitehead, and P.K. Moore The antinociceptive effect of 1-(2-trifluoromethylphenyl) imidazole (TRIM), a potent inhibitor of neuronal nitric oxide synthase in vitro, in the mouse Br. J. Pharmacol. 116 1995 2349 2350
39. R.L. Handy, and P.K. Moore A comparison of the effects of L-NAME, 7-NI and L-NIL on carrageenan-induced hindpaw edema and NOS activity Br. J. Pharmacol. 123 1998 1119 1126 (Pubitemid 28120509)
40. U.K. Hanisch, and H. Kettenmann Microglia: active sensor and versatile effector cells in the normal and pathologic brain Nat. Neurosci. 10 2007 1387 1394 (Pubitemid 350014685)
41. J.X. Hao, and X.J. Xu Treatment of a chronic allodynia-like response in spinally injured rats: effects of systemically administered nitric oxide synthase inhibitors Pain 66 1996 313 319
42. E.L. Heinzen, and G.M. Pollack Pharmacodynamics of morphine-induced neuronal nitric oxide production and antinociceptive tolerance development Brain Res. 1023 2004 175 184 (Pubitemid 39221420)
43. A. Hervera, R. Negrete, S. Leánez, J.M. Martín-Campos, and O. Pol The spinal cord expression of neuronal and inducible nitric oxide synthases and their contribution in the maintenance of neuropathic pain in mice PLoS ONE 5 2010 e14321
44. A. Hervera, R. Negrete, S. Leánez, J. Martín-Campos, and O. Pol The role of nitric oxide in the local antiallodynic and antihyperalgesic effects and expression of δ-opioid and cannabinoid-2 receptors during neuropathic pain in mice J. Pharmacol. Exp. Ther. 334 2010 887 896
45. A. Hervera, R. Negrete, S. Leánez, J.M. Martín-Campos, and O. Pol Peripheral effects of morphine and expression of μ-opioid receptors in the dorsal root ganglia during neuropathic pain: nitric oxide signaling Mol. Pain 12 2011 7 25
46. D.T. Hess, L.H. Lin, J.A. Freeman, and J.J. Norden Modification of cysteine residues within G(o) and other neuronal proteins by exposure to nitric oxide Neuropharmacology 33 1994 1283 1292
47. M.R. Hutchinson, B.D. Coats, S.S. Lewis, Y. Zhang, D.B. Sprunger, N. Rezvani, E.M. Baker, B.M. Jekich, J.L. Wieseler, A.A. Somogyi, D. Martin, S. Poole, C.M. Judd, S.F. Maier, and L.R. Watkins Proinflammatory cytokines oppose opioid-induced acute and chronic analgesia Brain Behav. Immun. 22 2008 1178 1189
48. T. Inoue, T. Mashimo, S. Shibuta, and I. Yoshiya Intrathecal administration of a new nitric oxide donor, NOC-18, produces acute thermal hyperalgesia in the rat J. Neurol. Sci. 153 1997 1 7 (Pubitemid 28010058)
49. H. Kakita, M. Aoyama, Y. Nagaya, H. Asai, M.H. Hussein, M. Suzuki, S. Kato, S. Saitoh, and K. Asai Diclofenac enhances proinflammatory cytokine-induced phagocytosis of cultured microglia via nitric oxide production Toxicol. Appl. Pharmacol. 268 2013 99 105
50. I. Kangrga, and M. Randić Outflow of endogenous aspartate and glutamate from the rat spinal dorsal horn in vitro by activation of low- and high-threshold primary afferent fibers. Modulation by μ-opioids Brain Res. 553 1991 347 352
51. Z. Khalil, and B. Khodr A role for free radicals and nitric oxide in delayed recovery in aged rats with chronic constriction nerve injury Free Radic. Biol. Med. 31 2001 430 439 (Pubitemid 32728430)
52. J.P. Kiss, and E.S. Vizi Nitric oxide: a novel link between synaptic and nonsynaptic transmission Trends Neurosci. 24 2001 211 215 (Pubitemid 32204376)
53. K.F. Kitto, J.E. Haley, and G.L. Wilcox Involvement of nitric oxide in spinally mediated hyperalgesia in the mouse Neurosci. Lett. 148 1992 1 5 (Pubitemid 23007690)
54. Y.A. Kolesnikov, C.G. Pick, G. Ciszewska, and G.W. Pasternak Blockade of tolerance to morphine but not to kappa opioids by a nitric oxide synthase inhibitor Proc. Natl. Acad. Sci. U. S. A. 90 1993 5162 5166 (Pubitemid 23182997)
55. K. Kuboyama, M. Tsuda, M. Tsutsui, Y. Toyohara, H. Tozaki-Saitoh, H. Shimokawa, N. Yanagihara, and K. Inoue Reduced spinal microglial activation and neuropathic pain after nerve injury in mice lacking all three nitric oxide synthases Mol. Pain 7 2011 50
56. C.J. LaBuda, M. Koblish, P. Tuthill, R.E. Dolle, and P. Little Antinociceptive activity of the selective iNOS inhibitor AR-C102222 in rodent models of inflammatory, neuropathic and post-operative pain Eur. J. Pain 10 2006 505 512 (Pubitemid 43947639)
57. D. Labuz, R. Przewlocki, and B. Przewlocka Cross-tolerance between the different mu-opioid receptor agonists endomorphin-1, endomorphin-2 and morphine at the spinal level in the rat Neurosci. Lett. 334 2002 127 130 (Pubitemid 35341638)
58. N.B. Lawand, W.D. Willis, and K.N. Westlund Blockade of joint inflammation and secondary hyperalgesia by L-NAME, a nitric oxide synthase inhibitor Neuroreport 8 1997 895 899 (Pubitemid 27152142)
59. L.M. Leite, A.G. Carvalho, P.L. Ferreira, I.X. Pessoa, D.O. Gonçalves, A. Lopes Ade, J.G. Góes, V.C. Alves, L.K. Leal, G.A. Brito, and G.S. Viana Anti-inflammatory properties of doxycycline and minocycline in experimental models: an in vivo and in vitro comparative study Inflammopharmacology 19 2011 99 110
60. D. Levy, and D.W. Zochodne Local nitric oxide synthase activity in a model of neuropathic pain Eur. J. Neurosci. 10 1998 1846 1855 (Pubitemid 28327330)
61. D. Levy, A. Höke, and D.W. Zochodne Local expression of inducible nitric oxide synthase in an animal model of neuropathic pain Neurosci. Lett. 260 1999 207 209 (Pubitemid 29089197)
62. D. Levy, P. Kubes, and D.W. Zochodne Delayed peripheral nerve degeneration, regeneration, and pain in mice lacking inducible nitric oxide synthase J. Neuropathol. Exp. Neurol. 60 2001 411 421 (Pubitemid 32467098)
63. J.C. Leza, I. Lizasoain, B. Cuéllar, M.A. Moro, and P. Lorenzo Correlation between brain nitric oxide synthase activity and opiate withdrawal Naunyn-Schmiedeberg's Arch. Pharmacol. 353 1996 349 354 (Pubitemid 26092051)
64. J.C. Leza, I. Lizasoain, O. San-Martín-Clark, and P. Lorenzo Morphine-induced changes in cerebral and cerebellar nitric oxide synthase activity Eur. J. Pharmacol. 285 1995 95 98
65. X. Li, and J. David Clark Chronic morphine exposure and the expression of heme oxygenase type 2 Brain Res. Mol. Brain Res. 75 2000 179 184 (Pubitemid 30109268)
66. X. Li, and J.D. Clark Spinal cord nitric oxide synthase and heme oxygenase limit morphine induced analgesia Brain Res. Mol. Brain Res. 95 2001 96 102 (Pubitemid 33000367)
67. Liu, D. Shenouda, T.V. Bilfinger, M.L. Stefano, H.I. Magazine, and G.B. Stefano Morphine stimulates nitric oxide release from invertebrate microglia Brain Res. 722 1996 125 131 (Pubitemid 26202931)
68. J.G. Liu, and K.J.S. Anand Protein kinases modulate the cellular adaptations associated with opioid tolerance and dependence Brain Res. Rev. 38 2001 1 19 (Pubitemid 34066494)
69. W. Liu, C.H. Wang, Y. Cui, L.Q. Mo, J.L. Zhi, S.N. Sun, Y.L. Wang, H.M. Yu, C.M. Zhao, J.Q. Feng, and P.X. Chen Inhibition of neuronal nitric oxide synthase antagonizes morphine antinociceptive tolerance by decreasing activation of p38 MAPK in the spinal microglia Neurosci. Lett. 410 2006 174 177 (Pubitemid 44750337)
70. D. Luo, S. Das, and R.S. Vincent Effects of methylene blue and LY83583 on neuronal nitric oxide synthase and NADPH-diaphorase Eur. J. Pharmacol. Mol. Pharmacol. Sec. 290 1995 247 251
71. H. Machelska, B. Ziolkowska, J. Mika, B. Przewlocka, and R. Przewlocki Chronic morphine increases biosynthesis of nitric oxide synthase in the rat spinal cord Neuroreport 8 1997 2743 2747 (Pubitemid 27373523)
72. H. Machelska, D. Labuz, R. Przewlocki, and B. Przewlocka Inhibition of nitric oxide synthase enhances antinociception mediated by mu, delta and kappa opioid receptors in acute and prolonged pain in the rat spinal cord J. Pharmacol. Exp. Ther. 282 1997 977 984 (Pubitemid 27340203)
73. H. Machelska, R. Przewłocki, M.W. Radomski, and B. Przewłocka Differential effects of intrathecally and intracerebroventricularly administered nitric oxide donors on noxious mechanical and thermal stimulation Pol. J. Pharmacol. 50 1998 407 415 (Pubitemid 29050567)
74. H.I. Magazine, Y. Liu, T.V. Bilfinger, G.L. Fricchione, and G.B. Stefano Morphine-induced conformational changes in immunocytes, endothelial cells and microglia are mediated by nitric oxide J. Immunol. 156 1996 4845 4850 (Pubitemid 26174471)
75. N.H. Majeed, B. Przewłocka, H. Machelska, and R. Przewłocki Inhibition of nitric oxide synthase attenuates the development of morphine tolerance and dependence in mice Neuropharmacology 33 1994 189 192 (Pubitemid 24104280)
76. A.B. Malmberg, and T.L. Yaksh Spinal nitric oxide synthesis inhibition blocks NMDA-induced thermal hyperalgesia and produces antinociception in the formalin test in rats Pain 54 1993 291 300 (Pubitemid 23259288)
77. C. Martucci, A.E. Trovato, B. Costa, E. Borsani, S. Franchi, V. Magnaghi, A.E. Panerai, L.F. Rodella, A.E. Valsecchi, P. Sacerdote, and M. Colleoni The purinergic antagonist PPADS reduces pain related behaviours and interleukin-1β, interleukin-6, iNOS and nNOS overproduction in central and peripheral nervous system after peripheral neuropathy in mice Pain 137 2008 81 95 (Pubitemid 351794401)
78. B. Mayer Biochemistry and molecular pharmacology of nitric oxide synthase S.R. Vincent, Nitric Oxide in the Nervous System 1995 Academic Press New York 21 42
79. H.J. McQuay Neuropathic pain: evidence matters Eur. J. Pain 6 Suppl. A 2002 11 18 (Review) (Pubitemid 40023564)
80. S.T. Meller, P.S. Pechman, G.F. Gebhart, and T.J. Maves Nitric oxide mediates the thermal hyperalgesia produced in a model of neuropathic pain in the rat Neuroscience 50 1992 7 10
81. S.T. Meller, C. Dykstra, and G.F. Gebhart Production of endogenous nitric oxide and activation of soluble guanylate cyclase are required for N-methyl-D-aspartate-produced facilitation of the nociceptive tail-flick reflex Eur. J. Pharmacol. 214 1992 93 96
82. S.T. Meller, and G.F. Gebhart Nitric oxide (NO) and nociceptive processing in the spinal cord Pain 52 1993 127 136 (Pubitemid 23068181)
83. S.T. Meller, C.P. Cummings, R.J. Traub, and G.F. Gebhart The role of nitric oxide in the development and maintenance of the hyperalgesia produced by intraplantar injection of carrageenan in the rat Neuroscience 60 1994 367 374 (Pubitemid 24175208)
84. S.T. Meller, C. Dykstra, D. Grzybycki, S. Murphy, and G.F. Gebhart The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat Neuropharmacology 33 1994 1471 1478 (Pubitemid 24353743)
85. J. Mika, M. Osikowicz, W. Makuch, and B. Przewlocka Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain Eur. J. Pharmacol. 560 2007 142 149 (Pubitemid 46341303)
86. J. Mika Modulation of microglia can attenuate neuropathic pain symptoms and enhance morphine effectiveness Pharmacol. Rep. 60 2008 297 307 (Review)
87. J. Mika, A. Wawrzczak-Bargiela, M. Osikowicz, W. Makuch, and B. Przewlocka Attenuation of morphine tolerance by minocycline and pentoxifylline in naive and neuropathic mice Brain Behav. Immun. 23 2009 75 84
88. L. Minghetti, and G. Levi Microglia as effector cells in brain damage and repair: focus on prostanoids and nitric oxide Prog. Neurobiol. 54 1998 99 125 (Pubitemid 28049822)
89. S. Moncada, R.M.J. Palmer, and E.A. Higgs Nitric oxide: physiology, pathophysiology and pharmacology Pharmacol. Rev. 43 1991 109 142
90. P.K. Moore, A. Oluyomi, R.C. Babbedge, P. Wallace, and S.L. Hart L-NG-nitro arginine methyl ester exhibits antinociceptive activity in the mouse Br. J. Pharmacol. 102 1991 198 202
91. P.K. Moore, P. Wallace, Z. Gaffen, S.L. Hart, and R.C. Babbedge Characterization of the novel nitric oxide synthase inhibitor 7-nitro indazole and related indazoles: antinociceptive and cardiovascular effects Br. J. Pharmacol. 110 1993 219 224 (Pubitemid 23257782)
92. A.K. Naik, S.K. Tandan, D. Kumar, and S.P. Dudhgaonkar Nitric oxide and its modulators in chronic constriction injury-induced neuropathic pain in rats Eur. J. Pharmacol. 530 2006 59 69 (Pubitemid 43037125)
93. M. Narita, T. Yoshida, and M. Nakajima Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice J. Neurochem. 97 2006 1337 1348 (Pubitemid 43725573)
94. C. Nathan, and Q.W. Xie Nitric oxide synthases: roles, tolls and controls Cell 78 1994 915 918 (Pubitemid 24292319)
95. C. Nathan Inducible nitric oxide synthase: what difference does it make J. Clin. Invest. 100 1997 2417 2423 (Pubitemid 27514879)
96. E.J. Nestler, and G.K. Aghajanian Molecular and cellular basis of addiction Science 278 1997 58 63 (Pubitemid 27446271)
97. R.A. North Opioid receptors and ion channels O.F.X. Almeida, T.S. Shippenberg, Neurobiology of Opioids 1991 Springer-Verlag New York 141 150
98. M.H. Ossipov, Y. Lopez, M.L. Nichols, D. Bian, and F. Porreca The loss of antinociceptive efficacy of spinal morphine in rats with nerve ligation injury is prevented by reducing spinal afferent drive Neurosci. Lett. 199 1995 87 90
99. M. Ozek, Y. Uresin, and M. Güngör Comparison of the effects of specific and nonspecific inhibition of nitric oxide synthase on morphine analgesia, tolerance and dependence in mice Life Sci. 72 2003 1943 1951 (Pubitemid 36207531)
100. I. Paakkari, and P. Lindsberg Nitric oxide in the central nervous system Annu. Mediaev. 27 1995 369 377
101. G.W. Pasternak, and P.J. Wood Multiple mu opiate receptors Life Sci. 38 1986 1889 1898 (Pubitemid 16012641)
102. G.W. Pasternak, Y.A. Kolesnikov, and A.M. Babey Perspectives on the N-methyl-D-aspartate/nitric oxide cascade and opioid tolerance Neuropsychopharmacology 13 1995 309 313 (Pubitemid 26008850)
103. M.B. Patel, C.N. Patel, V. Rajashekara, and B.C. Yoburn Opioid agonists differentially regulate mu-opioid receptors and trafficking proteins in vivo Mol. Pharmacol. 62 2002 1464 1470 (Pubitemid 35403842)
104. N.M. Perkins, and D.J. Tracey Hyperalgesia due to nerve injury: role of neutrophils Neurosci 101 2000 745 757
105. A. Pfeifer, B. Nürnberg, S. Kamm, M. Uhde, G. Schultz, P. Ruth, and F. Hofmann Cyclic GMP-dependent protein kinase blocks pertussis toxin-sensitive hormone receptor signaling pathways in Chinese hamster ovary cells J. Biol. Chem. 270 1995 9052 9059
106. J. Pineda, J.H. Kogan, and G.K. Aghajanian Nitric oxide and carbon monoxide activate locus coeruleus neurons through a cGMP-dependent protein kinase: involvement of a nonselective cationic channel J. Neurosci. 16 1996 1389 1399 (Pubitemid 26145919)
107. F. Porreca, Q.B. Tang, D. Bian, M. Riedl, R. Elde, and J. Lai Spinal opioid mu receptor expression in lumbar spinal cord of rats following nerve injury Brain Res. 795 1998 197 203 (Pubitemid 28337831)
108. H. Prast, and A. Philippu Nitric oxide as modulator of neuronal function Prog. Neurobiol. 64 2001 51 68 (Pubitemid 32201889)
109. B. Przewlocka, J. Mika, D. Labuz, G. Toth, and R. Przewłocki Spinal analgesic action of endomorphins in acute, inflammatory and neuropathic pain in rats Eur. J. Pharmacol. 367 1999 189 196 (Pubitemid 29106370)
110. R. Przewlocki, H. Machelska, and B. Przewlocka Inhibition of nitric oxide synthase enhances morphine antinociception in the rat spinal cord Life Sci. 53 1993 PL1 5
111. R. Przewłocki, D. Labuz, J. Mika, B. Przewłocka, C. Tomboly, and G. Toth Pain inhibition by endomorphins Ann. N. Y. Acad. Sci. 897 1999 154 164 (Pubitemid 30040328)
112. R. Przewlocki, and B. Przewlocka Opioids in chronic pain Eur. J. Pharmacol. 429 2001 79 91 (Review) (Pubitemid 33043984)
113. R. Przewlocki, and B. Przewlocka Opioids in neuropathic pain Curr. Pharm. Des. 11 2005 3013 3025 (Review) (Pubitemid 41158089)
114. S. Pu, T.L. Horvath, S. Diano, F. Naftolin, P.S. Kalra, and S.P. Kalra Evidence showing that beta-endorphin regulates cyclic guanosine 3',5'-monophosphate (cGMP) efflux: anatomical and functional support for an interaction between opiates and nitric oxide Endocrinology 138 1997 1537 1543 (Pubitemid 27137104)
115. W. Riedel, and G. Neeck Nociception, pain, and antinociception: current concepts Z. Rheumatol. 60 2001 404 415 (Pubitemid 34066644)
116. A. Romero, L. Hernández, P. García-Nogales, and M.M. Puig Deletion of the inducible nitric oxide synthase gene reduces peripheral morphine tolerance in a mouse model of chronic inflammation Fundam. Clin. Pharmacol. 24 2010 317 323
117. G. Sakaue, M. Shimaoka, T. Fukuoka, T. Hiroi, T. Inoue, N. Hashimoto, T. Sakaguchi, Y. Sawa, R. Morishita, H. Kiyono, K. Noguchi, and T. Mashimo NF-kappa B decoy suppresses cytokine expression and thermal hyperalgesia in a rat neuropathic pain model NeuroReport 12 2001 2079 2084 (Pubitemid 32646249)
118. D. Salvemini, Z.Q. Wang, D.M. Bourdon, M.K. Stern, M.G. Currie, and P.T. Manning Evidence of peroxynitrite involvement in the carrageenan-induced rat paw oedema Eur. J. Pharmacol. 303 1996 217 220 (Pubitemid 26200675)
119. M. Satoh, and Y. Kuraishi Opioid interactions with other neuropeptides in the spinal cord: relevance to nociception O.F.X. Almeida, T.S. Shippenberg, Neurobiology of Opioids 1991 Springer-Verlag New York 261 271
120. E.M. Schuman, M.K. Meffert, H. Schulman, and D.V. Madison An ADP-ribosyltransferase as a potential target for nitric oxide action in hippocampal long-term potentiation Proc. Natl. Acad. Sci. U. S. A. 91 1994 11958 11962 (Pubitemid 24368583)
121. S. Shibuta, T. Mashimo, A. Ohara, P. Zhang, and I. Yoshiya Intracerebroventricular administration of a nitric oxide-releasing compound, NOC-18, produces thermal hyperalgesia in rats Neurosci. Lett. 187 1995 103 106
122. S.H. Snyder Nitric oxide: first in a new class of neurotransmitters Science 257 1992 494 496
123. C. Speth, M.P. Dierich, and P. Gasque Neuroinvasion by pathogens: a key role of the complement system Mol. Immunol. 38 2002 669 679 (Pubitemid 34164184)
124. G.B. Stefano, A. Hartman, T.V. Bilfinger, H.I. Magazine, Y. Liu, F. Casares, and M.S. Goligorsky Presence of the mu3 opiate receptor in endothelial cells. Coupling to nitric oxide production and vasodilation J. Biol. Chem. 270 1995 30290 30293
125. G.B. Stefano, M. Salzet, H.I. Magazine, and T.V. Bilfinger Antagonism of LPS and IFN-gamma induction of iNOS in human saphenous vein endothelium by morphine and anandamide by nitric oxide inhibition of adenylate cyclase J. Cardiovasc. Pharmacol. 31 1998 813 820 (Pubitemid 28265289)
126. G.B. Stefano, Y. Goumon, T.V. Bilfinger, I.D. Welters, and P. Cadet Basal nitric oxide limits immune, nervous and cardiovascular excitation: human endothelia express a mu opiate receptor Prog. Neurobiol. 60 2000 513 530 (Pubitemid 30100397)
127. C.S. Sung, Z.H. Wen, W.K. Chang, S.T. Ho, S.K. Tsai, Y.C. Chang, and C.S. Wong Intrathecal interleukin-1beta administration induces thermal hyperalgesia by activating inducible nitric oxide synthase expression in the rat spinal cord Brain Res. 1015 2004 145 153
128. Q. Tang, C.I. Svensson, B. Fitzsimmons, M. Webb, T.L. Yaksh, and X.Y. Hua Inhibition of spinal constitutive NOS-2 by 1400W attenuates tissue injury and inflammation-induced hyperalgesia and spinal p38 activation Eur. J. Neurosci. 25 2007 2964 2972 (Pubitemid 46888819)
129. R.Z. Terwilliger, J. Ortiz, X. Guitart, and E.J. Nestler Chronic morphine administration increases beta-adrenergic receptor kinase (beta ARK) levels in the rat locus coeruleus J. Neurochem. 63 1994 1983 1986 (Pubitemid 24326247)
130. J.A. Trafton, C. Abbadie, K. Marek, and A.I. Basbaum Postsynaptic signaling via the [mu]-opioid receptor: responses of dorsal horn neurons to exogenous opioids and noxious stimulation Neurosci 20 2000 8578 8584
131. K.A. Trujillo The neurobiology of opiate tolerance, dependence and sensitization: mechanisms of NMDA receptor-dependent synaptic plasticity Neurotox. Res. 4 2002 373 391
132. V. Vacca, S. Marinelli, S. Luvisetto, and F. Pavone Botulinum toxin A increases analgesic effects of morphine, counters development of morphine tolerance and modulates glia activation and μ opioid receptor expression in neuropathic mice Brain Behav. Immun. 32 2013 40 50 10.1016/j.bbi.2013.01.088
133. E.J. Van Bockstaele, and K.G. Commons Internalization of mu-opioid receptors produced by etorphine in the rat locus coeruleus Neuroscience 108 2001 467 477 (Pubitemid 34037891)
134. R. Watkins, M.R. Hutchinson, I.N. Johnston, and S.F. Maier Glia: novel counter-regulators of opioid analgesia Trends Neurosci. 28 2005 661 669 (Pubitemid 41654390)
135. L.R. Watkins, M.R. Hutchinson, A. Ledeboer, J. Wieseler-Frank, E.D. Milligan, and S.F. Maier Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids Brain Behav. Immun. 21 2007 131 146 (Pubitemid 46038918)
136. M.J. Wilderman, and W.M. Armstead Role of neuronal NO synthase in relationship between NO and opioids in hypoxia-induced pial artery dilation Am. J. Phys. 273 1997 H1807 H1815
137. M.J. Wilderman, and W.M. Armstead Role of endothelial nitric oxide synthase in hypoxia-induced pial artery dilation J. Cereb. Blood Flow Metab. 18 1998 531 538 (Pubitemid 28213537)
138. C.S. Wong, C.H. Cherng, and C.S. Tung Intrathecal administration of excitatory amino acid receptor antagonists or nitric oxide synthase inhibitor reduced autotomy behavior in rats Anesth. Analg. 87 1998 605 608
139. C.S. Wong, M.M. Hsu, Y.Y. Chou, P.L. Tao, and C.S. Tung Morphine tolerance increases [3H]MK-801 binding affinity and constitutive neuronal nitric oxide synthase expression in rat spinal cord Br. J. Anaesth. 85 2000 587 591
140. W. Wu Expression of nitric-oxide synthase (NOS) in injured CNS neurons as shown by NADPH diaphorase histochemistry Exp. Neurol. 120 1993 153 159 (Pubitemid 23165010)
141. J.Y. Xu, and L.F. Tseng Increase of nitric oxide by L-arginine potentiates beta-endorphin- but not mu-, delta- or kappa-opioid agonist-induced antinociception in the mouse Eur. J. Pharmacol. 236 1993 137 142 (Pubitemid 23146860)
142. J.Y. Xu, and L.F. Tseng Nitric oxide/cyclic guanosine monophosphate system in the spinal cord differentially modulates intracerebroventricularly administered morphine- and beta-endorphin-induced antinociception in the mouse J. Pharmacol. Exp. Ther. 274 1995 8 16
143. Z.Q. Xu, J. de Vente, H. Steinbusch, S. Grillner, and T. Hokfelt The NO-cGMP pathway in the rat locus coeruleus: electrophysiological, immunohistochemical and in situ hybridization studies Eur. J. Neurosci. 10 1998 3508 3516
144. T.L. Yaksh, and T.A. Rudy Chronic catheterization of the spinal subarachnoid space Physiol. Behav. 17 1976 1031 1036 (Pubitemid 8063691)
145. H. Yamaguchi, and H. Naito Antinociceptive synergistic interaction between morphine and n omega-nitro L-arginine methyl ester on thermal nociceptive tests in the rats Can. J. Anaesth. 43 1996 975 981
146. T. Yamamoto, and N. Shimoyama Role of nitric oxide in the development of thermal hyperesthesia induced by sciatic nerve constriction injury in the rat Anesthesiology 82 1995 1266 1273
147. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110 (Pubitemid 13058546)